From the royal charter to Bishop Varlaam of Suzdal in 1578, it follows that on the site of the Boris and Gleb Church there was previously a monastery of the same name and the Borisova Side settlement. However, in the inventory of the city of Suzdal from 1617, there are no mentions of the Boris and Gleb Monastery and its settlement. It is likely that this place was destroyed and devastated during the Polish intervention in the Time of Troubles. The land survey book of Suzdal from 1628-1629 reports that across the Kamenka River there was the Boris and Gleb Monastery of Archbishop Joseph, which had the Church of the Annunciation of the Mother of God and the Church of St. Nicholas the Wonderworker, made of wood.

The exact date of the church's construction is unknown, but it is believed to have been built in 1749. However, based on architectural features such as the octagon on a square base and Baroque elements on the facades, the church can be attributed to the late 17th century, while the bell tower dates to the mid-18th century. The church is located in the Zarechnaya side on Borisova Side Street and is also known as the Istochnikovskaya Church.

In 1923, the church was closed, and the Suzdal Museum proposed to demolish it for construction materials, including for the city bathhouse. The Winter St. Nicholas Church of 1718, located northwest of Boris and Gleb Church, was dismantled by 1937. The Summer Boris and Gleb Church avoided demolition. The church remained abandoned for a long time; it was planned to be used as a warehouse, but in 1961 it was restored under the guidance of A. D. Varganov as part of the transformation of Suzdal into a museum city.

In the early 2000s, the Boris and Gleb Church was transferred to the Russian Orthodox Autonomous Church, but restoration did not begin. On June 10, 2014, the church came under the jurisdiction of the Vladimir Diocese of the Russian Orthodox Church.

In the summer of 2017, a major restoration of the severely dilapidated church began. The building received updated cladding, as well as a new gilded dome and spire. By 2019, the exterior appearance of the church was restored, and the adjacent territory was improved.

The red brick church is built in the style of Moscow Baroque, which is atypical for Suzdal. An apse and a low refectory are attached to the main building, which is in the form of an octagon on a powerful square base, along with a four-sided bell tower with a spire and large openings in the tiers of the bells. The building is decorated with carved window frames, pilasters, and a portal, and inside, frescoes from the 18th and 19th centuries have been preserved.